Hypoxia-induced SETX links replication stress with the unfolded protein response

Tumour hypoxia is associated with poor patient prognosis and therapy resistance. A unique transcriptional response is initiated by hypoxia which includes the rapid activation of numerous transcription factors in a background of reduced global transcription. Here, we show that the biological response...

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Veröffentlicht in:Nature communications Jg. 12; H. 1; S. 3686 - 14
Hauptverfasser: Ramachandran, Shaliny, Ma, Tiffany S., Griffin, Jon, Ng, Natalie, Foskolou, Iosifina P., Hwang, Ming-Shih, Victori, Pedro, Cheng, Wei-Chen, Buffa, Francesca M., Leszczynska, Katarzyna B., El-Khamisy, Sherif F., Gromak, Natalia, Hammond, Ester M.
Format: Journal Article
Sprache:Englisch
Veröffentlicht: London Nature Publishing Group UK 17.06.2021
Nature Publishing Group
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Activating Transcription Factor 4 - genetics
Activating Transcription Factor 4 - metabolism
Cell Death - drug effects
Cell Death - genetics
Cell Hypoxia
Cell Line, Tumor
Cell Survival - drug effects
Cell Survival - genetics
Chromatin Immunoprecipitation
Damage accumulation
Deoxyribonucleic acid
DNA
DNA biosynthesis
DNA damage
DNA Damage - genetics
DNA helicase
DNA Helicases - genetics
DNA Helicases - metabolism
eIF-2 Kinase - metabolism
Gene Expression Regulation - drug effects
Gene Expression Regulation - genetics
Humanities and Social Sciences
Humans
Hypoxia
Mammalian cells
multidisciplinary
Multifunctional Enzymes - genetics
Multifunctional Enzymes - metabolism
Nucleic Acid Synthesis Inhibitors - pharmacology
Oxygen - pharmacology
Protein folding
Proteins
R-Loop Structures - drug effects
R-Loop Structures - genetics
R-loops
Replication
Ribonucleic acid
RNA
RNA helicase
RNA Helicases - genetics
RNA Helicases - metabolism
RNA-Seq
Science
Science (multidisciplinary)
Transcription activation
Transcription factors
Tumors
Unfolded Protein Response - drug effects
Unfolded Protein Response - genetics
Up-Regulation
Zinostatin - pharmacology
ISSN:2041-1723, 2041-1723
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Abstract Tumour hypoxia is associated with poor patient prognosis and therapy resistance. A unique transcriptional response is initiated by hypoxia which includes the rapid activation of numerous transcription factors in a background of reduced global transcription. Here, we show that the biological response to hypoxia includes the accumulation of R-loops and the induction of the RNA/DNA helicase SETX. In the absence of hypoxia-induced SETX, R-loop levels increase, DNA damage accumulates, and DNA replication rates decrease. Therefore, suggesting that, SETX plays a role in protecting cells from DNA damage induced during transcription in hypoxia. Importantly, we propose that the mechanism of SETX induction in hypoxia is reliant on the PERK/ATF4 arm of the unfolded protein response. These data not only highlight the unique cellular response to hypoxia, which includes both a replication stress-dependent DNA damage response and an unfolded protein response but uncover a novel link between these two distinct pathways. Hypoxia induces a change in transcriptional response in mammalian cells. Here the authors reveal a role for the RNA/DNA helicase Senataxin in protecting cells from DNA damage induced during transcription in hypoxia.
AbstractList Tumour hypoxia is associated with poor patient prognosis and therapy resistance. A unique transcriptional response is initiated by hypoxia which includes the rapid activation of numerous transcription factors in a background of reduced global transcription. Here, we show that the biological response to hypoxia includes the accumulation of R-loops and the induction of the RNA/DNA helicase SETX. In the absence of hypoxia-induced SETX, R-loop levels increase, DNA damage accumulates, and DNA replication rates decrease. Therefore, suggesting that, SETX plays a role in protecting cells from DNA damage induced during transcription in hypoxia. Importantly, we propose that the mechanism of SETX induction in hypoxia is reliant on the PERK/ATF4 arm of the unfolded protein response. These data not only highlight the unique cellular response to hypoxia, which includes both a replication stress-dependent DNA damage response and an unfolded protein response but uncover a novel link between these two distinct pathways.Hypoxia induces a change in transcriptional response in mammalian cells. Here the authors reveal a role for the RNA/DNA helicase Senataxin in protecting cells from DNA damage induced during transcription in hypoxia.
Tumour hypoxia is associated with poor patient prognosis and therapy resistance. A unique transcriptional response is initiated by hypoxia which includes the rapid activation of numerous transcription factors in a background of reduced global transcription. Here, we show that the biological response to hypoxia includes the accumulation of R-loops and the induction of the RNA/DNA helicase SETX. In the absence of hypoxia-induced SETX, R-loop levels increase, DNA damage accumulates, and DNA replication rates decrease. Therefore, suggesting that, SETX plays a role in protecting cells from DNA damage induced during transcription in hypoxia. Importantly, we propose that the mechanism of SETX induction in hypoxia is reliant on the PERK/ATF4 arm of the unfolded protein response. These data not only highlight the unique cellular response to hypoxia, which includes both a replication stress-dependent DNA damage response and an unfolded protein response but uncover a novel link between these two distinct pathways.
Tumour hypoxia is associated with poor patient prognosis and therapy resistance. A unique transcriptional response is initiated by hypoxia which includes the rapid activation of numerous transcription factors in a background of reduced global transcription. Here, we show that the biological response to hypoxia includes the accumulation of R-loops and the induction of the RNA/DNA helicase SETX. In the absence of hypoxia-induced SETX, R-loop levels increase, DNA damage accumulates, and DNA replication rates decrease. Therefore, suggesting that, SETX plays a role in protecting cells from DNA damage induced during transcription in hypoxia. Importantly, we propose that the mechanism of SETX induction in hypoxia is reliant on the PERK/ATF4 arm of the unfolded protein response. These data not only highlight the unique cellular response to hypoxia, which includes both a replication stress-dependent DNA damage response and an unfolded protein response but uncover a novel link between these two distinct pathways. Hypoxia induces a change in transcriptional response in mammalian cells. Here the authors reveal a role for the RNA/DNA helicase Senataxin in protecting cells from DNA damage induced during transcription in hypoxia.
Tumour hypoxia is associated with poor patient prognosis and therapy resistance. A unique transcriptional response is initiated by hypoxia which includes the rapid activation of numerous transcription factors in a background of reduced global transcription. Here, we show that the biological response to hypoxia includes the accumulation of R-loops and the induction of the RNA/DNA helicase SETX. In the absence of hypoxia-induced SETX, R-loop levels increase, DNA damage accumulates, and DNA replication rates decrease. Therefore, suggesting that, SETX plays a role in protecting cells from DNA damage induced during transcription in hypoxia. Importantly, we propose that the mechanism of SETX induction in hypoxia is reliant on the PERK/ATF4 arm of the unfolded protein response. These data not only highlight the unique cellular response to hypoxia, which includes both a replication stress-dependent DNA damage response and an unfolded protein response but uncover a novel link between these two distinct pathways.Tumour hypoxia is associated with poor patient prognosis and therapy resistance. A unique transcriptional response is initiated by hypoxia which includes the rapid activation of numerous transcription factors in a background of reduced global transcription. Here, we show that the biological response to hypoxia includes the accumulation of R-loops and the induction of the RNA/DNA helicase SETX. In the absence of hypoxia-induced SETX, R-loop levels increase, DNA damage accumulates, and DNA replication rates decrease. Therefore, suggesting that, SETX plays a role in protecting cells from DNA damage induced during transcription in hypoxia. Importantly, we propose that the mechanism of SETX induction in hypoxia is reliant on the PERK/ATF4 arm of the unfolded protein response. These data not only highlight the unique cellular response to hypoxia, which includes both a replication stress-dependent DNA damage response and an unfolded protein response but uncover a novel link between these two distinct pathways.
Hypoxia induces a change in transcriptional response in mammalian cells. Here the authors reveal a role for the RNA/DNA helicase Senataxin in protecting cells from DNA damage induced during transcription in hypoxia.
ArticleNumber 3686
Author Griffin, Jon
Ramachandran, Shaliny
Leszczynska, Katarzyna B.
Foskolou, Iosifina P.
Cheng, Wei-Chen
Hammond, Ester M.
Gromak, Natalia
Ma, Tiffany S.
Victori, Pedro
Hwang, Ming-Shih
Ng, Natalie
Buffa, Francesca M.
El-Khamisy, Sherif F.
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  organization: Department of Molecular Biology and Biotechnology, Healthy Lifespan and Neuroscience Institute, Firth Court, University of Sheffield, Department of Histopathology, Sheffield Teaching Hospitals NHS Foundation Trust
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  surname: Hammond
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/34140498$$D View this record in MEDLINE/PubMed
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Snippet Tumour hypoxia is associated with poor patient prognosis and therapy resistance. A unique transcriptional response is initiated by hypoxia which includes the...
Hypoxia induces a change in transcriptional response in mammalian cells. Here the authors reveal a role for the RNA/DNA helicase Senataxin in protecting cells...
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pubmedcentral
proquest
pubmed
crossref
springer
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Open Access Repository
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Publisher
StartPage 3686
SubjectTerms 13/1
13/106
13/51
49/109
49/88
49/90
49/91
631/337
631/67
631/80
82/29
82/80
96/63
Activating Transcription Factor 4 - genetics
Activating Transcription Factor 4 - metabolism
Cell Death - drug effects
Cell Death - genetics
Cell Hypoxia
Cell Line, Tumor
Cell Survival - drug effects
Cell Survival - genetics
Chromatin Immunoprecipitation
Damage accumulation
Deoxyribonucleic acid
DNA
DNA biosynthesis
DNA damage
DNA Damage - genetics
DNA helicase
DNA Helicases - genetics
DNA Helicases - metabolism
eIF-2 Kinase - metabolism
Gene Expression Regulation - drug effects
Gene Expression Regulation - genetics
Humanities and Social Sciences
Humans
Hypoxia
Mammalian cells
multidisciplinary
Multifunctional Enzymes - genetics
Multifunctional Enzymes - metabolism
Nucleic Acid Synthesis Inhibitors - pharmacology
Oxygen - pharmacology
Protein folding
Proteins
R-Loop Structures - drug effects
R-Loop Structures - genetics
R-loops
Replication
Ribonucleic acid
RNA
RNA helicase
RNA Helicases - genetics
RNA Helicases - metabolism
RNA-Seq
Science
Science (multidisciplinary)
Transcription activation
Transcription factors
Tumors
Unfolded Protein Response - drug effects
Unfolded Protein Response - genetics
Up-Regulation
Zinostatin - pharmacology
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Title Hypoxia-induced SETX links replication stress with the unfolded protein response
URI https://link.springer.com/article/10.1038/s41467-021-24066-z
https://www.ncbi.nlm.nih.gov/pubmed/34140498
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https://pubmed.ncbi.nlm.nih.gov/PMC8211819
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Volume 12
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